Prevalence of Listeria monocytogenes in dairy products in Turkey: A Meta-Analysis

Öz

This study was aimed to conduct a meta-analysis to determine the seroprevalence of Listeria monocytogenes in dairy products in Turkey. A systematic literature search was conducted using the Medline/PubMed, Science Direct, Web of Science, and Scopus databases to identify studies reporting the seroprevalence of L. monocytogenes in dairy products. The search was conducted using the following keywords: (“ice cream” or “curd” or “cream” or “cheese” or “butter” or “yoğurt” or “dairy” or “milk”) and (“Listeriosis” or “Listeria monocytogenes” or “Listeria”) and (“Turkiye” or “Turkey”) and (“seropositivity” or “seroprevalence” or “prevalence”). A comprehensive meta-analysis included a total of 4766 dairy products from the 27 studies. The overall molecular prevalence of Listeria monocytogenes in dairy products in Turkey was estimated to be 7.4% (95% confidence interval [CI]: 4.7-10.7%). The I2 value of 93.5% (CI95%91.6–95.0) suggested high heterogeneity, with a τ2 of 3.4422 (CI95%-1.7091–8.5936), and an X2 statistic of 399.2 (P < 0.0001). In conclusion, this meta-analysis reveals a significant seroprevalence of L. monocytogenes in dairy products in Turkey. The findings highlight the need for improved control measures to minimize the risk of contamination and ensure consumer safety. By implementing rigorous hygiene practices, enhancing monitoring systems, and promoting collaborative efforts between industry and regulatory bodies, the dairy sector in Turkey can effectively mitigate the risks associated with L. monocytogenes and maintain high standards of food safety.

Anahtar Kelimeler

• cheese
• dairy
• milk
• prevalence

Etik Beyan

not necessary

Teşekkür

Not applicable

Kaynakça

1. Abay, S., Aydin, F., & Sumerkan, A. B. (2012). Molecular typing of Listeria spp. isolated from different sources. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 59(3), 183-190.
2. Akin, A. C., Arikan, M. S., Polat, M., Mat, B., Cevrimli, M. B., Demirsöz, M., & Tekindal, M. A. (2022). Examining the production amount of milk and dairy products using network analysis in Turkey. Food Science and Technology, 42, e125821. https://doi.org/10.1590/fst.125821
3. Aksoy, A., Sezer, Ç., Vatansever, L., & Gülbaz, G. (2018). Presence and antibiotic resistance of Listeria monocytogenes in raw milk and dairy products. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(3), 415-421. https://doi.org/10.9775/kvfd.2017.19081
4. Andersson, C., Gripenland, J., & Johansson, J. (2015). Using the chicken embryo to assess virulence of Listeria monocytogenes and to model other microbial infections. Nature Protocols, 10: 1155–1164. https://doi.org/10.1038/nprot.2015.073
5. Arslan, S., & Ozdemir, F. (2020). Prevalence and antimicrobial resistance of Listeria species and molecular characterization of Listeria monocytogenes isolated from retail ready-to-eat foods. FEMS Microbiology Letters, 367(4), fnaa006. https://doi.org/10.1093/femsle/fnaa006
6. Arslan, S., & Ozdemir, F. (2008). Prevalence and antimicrobial resistance of Listeria spp. in homemade white cheese. Food control, 19(4), 360-363. https://doi.org/10.1016/j.foodcont.2007.04.009.
7. Aydın, R., Gökmen, M., Kara, R., Önen, A., & Ektik, N. (2019). The prevalence and molecular characterization of Listeria monocytogenes in corn silage, feces and bulk tank milk samples in dairy cattle farms in Balikesir, Turkey. Israel Journal of Veterinary Medicine, 74(4): 184-189.
8. Aygun, O., & Pehlivanlar, S. (2006). Listeria spp. in the raw milk and dairy products in Antakya, Turkey. Food Control, 17(8), 676-679. https://doi.org/10.1016/j.foodcont.2005.09.014.

9. Babacan, O. (2020). Antibiotic susceptibility and phylogenetic analyses for the origins and serotypes of Listeria monocytogenes strains isolated from ice cream and cream cakes. Turkish Journal of Veterinary & Animal Sciences, 44(5), 1100-1109. https://doi.org/10.3906/vet-2003-116
10. Bor, Ö. (2014). Economics of Dairy Farming in Turkey, International Journal of Food and Agricultural Economics, 2: 49-62. https://doi.org/10.22004/ag.econ.190811.
11. Borenstein, M., Hedges, L. V., Higgins, J. P., & Rothstein, H. R. (2021). Introduction to meta-analysis. John Wiley & Sons.
12. Bouras, E., Tsilidis, K. K., Pounis, G., & Haidich, A. B. (2019). Meta-analysis of nutrition studies. Analysis in nutrition research, 163-196. https://doi.org/10.1016/B978-0-12-814556-2.00007-5
13. Cagri-Mehmetoglu, A., Yaldirak, G., Bodur, T., Simsek, M., Bozkir, H., & Eren, N. M. (2011). Incidence of Listeria monocytogenes and Escherichia coli O157: H7 in two Kasar Cheese processing environments. Food Control, 22(5), 762-766. https://doi.org/10.1016/j.foodcont.2010.11.011
14. Cetinkaya, F., Elal Mus, T., Yibar, A., Guclu, N., Tavsanli, H., & Cibik, R. (2014). Prevalence, serotype identification by multiplex polymerase chain reaction and antimicrobial resistance patterns of Listeria monocytogenes isolated from retail foods. Journal of food safety, 34(1), 42-49. https://doi.org/10.1111/jfs.12093
15. Cetinkaya, F., & Soyutemiz, G. E. (2007). Evaluation of Listeria monocytogenes populations during the manufacture and vacuum-packaged storage of kashar cheese. Acta Veterinaria Brno, 76(1), 143-148. https://doi.org/10.2754/avb200776010143
16. Cokal, Y., Dagdelen, A., Cenet, O., & Gunsen, U. (2012). Presence of L. monocytogenes and some bacterial pathogens in two Turkish traditional foods, Mihalic cheese and Hosmerim dessert. Food Control, 26(2), 337-340. https://doi.org/10.1016/j.foodcont.2012.01.058
17. Colak, H., Hampikyan, H., Bingol, E. B., & Ulusoy, B. (2007). Prevalence of L. monocytogenes and Salmonella spp. in tulum cheese. Food Control, 18(5), 576-579. https://doi.org/10.1016/j.foodcont.2006.02.004
18. Cossart, P. (2011). Illuminating the landscape of host–pathogen interactions with the bacterium Listeria monocytogenes. Proceedings of the National Academy of Sciences, United States of America, 108(49), 19484–19491. https://doi.org/10.1073/pnas.1112371108
19. Durmaz, H., Avci, M., & Aygün, O. (2015). The presence of Listeria species in corn silage and raw milk produced in Southeast Region of Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 21(1), 41-44. https://doi.org/10.9775/kvfd.2014.11664
20. Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) Bias in meta- analysis detected by a simple, graphical test. BMJ, 315(7109), pp. 629-634. https://doi.org/10.1136/bmj.315.7109.629
21. Ekici, G., Dümen, E., Bayrakal, G. M., & Ergin, S. (2019). Molecular identification of Listeria monocytogenes and Escherichia coli O157: H7 isolated from fresh kashar cheese and milk creme. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 25(2), 215-219. https://doi.org/10.9775/kvfd.2018.20702
22. Falardeau, J., Trmčić, A., & Wang, S. (2021). The occurrence, growth, and biocontrol of Listeria monocytogenes in fresh and surface‐ripened soft and semisoft cheeses. Comprehensive Reviews in Food Science and Food Safety, 20(4), 4019-4048. https://doi.org/10.1111/1541-4337.12768
23. Gulel, G. T., Gucukoglu, A., Cadirci, O., Saka, E., & Alisarli, M. (2020). Serotyping and antibiotic resistance of Listeria monocytogenes isolated from raw water buffalo milk and milk products. Journal of Food Science, 85(9), 2889-2895. https://doi.org/10.1111/1750-3841.15376
24. Guner, A., & Telli, N. (2011). A survey on the presence of Listeria monocytogenes in various semi-hard cheeses from different regions of Turkey. Journal of Animal and Veterinary Advances, 10(14), 1890-4. https://doi.org/10.3923/javaa.2011.1890.1894
25. Jiang, X., Jiang, C., Yu, T., Jiang, X., Kang, R., Ren, S., Chen, H., Zhang, Y., Li, Y., Meng, H., & Wang, H. (2022). Phenyllactic acid application to control Listeria monocytogenes biofilms and its growth in milk and spiced beef. International Journal of Food Microbiology, 381, 109910. https://doi.org/10.1016/j.ijfoodmicro.2022.109910
26. Kahraman, T., Ozmen, G., Ozinan, B., & Omer Goksoy, E. (2010). Prevalence of Salmonella spp. and Listeria monocytogenes in different cheese types produced in Turkey. British Food Journal, 112(11), 1230-1236. https://doi.org/10.1108/00070701011088214
27. Karadal, F., & Yildirim, Y. (2014). Antimicrobial susceptibility and serotype distribution of Listeria monocytogenes isolates obtained from raw milk cheese samples sold in Nigde. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 61(4), 255-260. https://doi.org/10.1501/Vetfak_0000002639
28. Kelley, G. A., & Kelley, K. S. (2019). Systematic reviews and meta-analysis in nutrition research. British Journal of Nutrition, 122(11), 1279-1294. https://doi.org/10.1017/S0007114519002241
29. Kevenk, T. O., & Gulel, G. T. (2016). Prevalence, antimicrobial resistance and serotype distribution of Listeria monocytogenes isolated from raw milk and dairy products. Journal of Food Safety, 36(1), 11-18. https://doi.org/10.1111/jfs.12208
30. Kevenk, T. O., & Koluman, A. (2022). Seasonal effect on L. monocytogenes prevalence in meat and dairy products assessed by VIDAS LMO2 and ISO 11290: 1 methods. International Food Research Journal 29(4), 929 – 936. https:/dx.doi.org/10.47836/ifrj.29.4.20
31. Lee, Y. H. (2019). Strengths and limitations of meta-analysis. The Korean Journal of Medicine, 94(5), 391-395. https://doi.org/10.3904/kjm.2019.94.5.391
32. Matyar, F., Guzeldag, G., & Mercimek, H. A. (2010). Multiple antibiotic resistance among Listeria monocytogenes in retail foods, in Adana, Turkey. Italian Journal of Food Science, 22(4), 467-472.
33. Mazaheri, T., Cervantes-Huamán, B. R., Bermúdez-Capdevila, M., Ripolles-Avila, C., & Rodríguez-Jerez, J. J. (2021). Listeria monocytogenes biofilms in the food industry: is the current hygiene program sufficient to combat the persistence of the pathogen? Microorganisms, 9(1), 181. https://doi.org/10.3390/microorganisms9010181
34. Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Prisma Group, T. (2009). Preferred reporting items for systematic reviews and meta-analyses: the Prisma statement. Annals of internal medicine, 151(4), 264-269. https://doi.org/10.7326/0003-4819-151-4-200908180-00135
35. Nardi, V. A. M., Teixeira, R., Ladeira, W. J., & de Oliveira Santini, F. (2020). A meta-analytic review of food safety risk perception. Food Control, 112, 107089. https://doi.org/10.1016/j.foodcont.2020.107089
36. Ntuli, V., Sibanda, T., Elegbeleye, J. A., Mugadza, D. T., Seifu, E., & Buys, E. M. (2023). Dairy production: microbial safety of raw milk and processed milk products. In Present Knowledge in Food Safety (pp. 439-454). Academic Press.
37. Oktem, A. B., Bayram, G., Ceylan, A. E., & Yentur, G. (2006). Prevalence of Listeria monocytogenes in some Turkish foodstuffs. Journal of food quality, 29(1), 76-86. https://doi.org/10.1111/j.1745-4557.2006.00057.x
38. Ramaswarmy, V., Cresence, V. M., Rejitha, J. S., Lekshmi, M. U., Dharsana, K. S., Prasad, S. P. & Vijila, H. M. (2007). Listeria–review of epidemiology and pathogenesis. Journal of Microbiology Immunology and Infection, 40(1), 4–13.
39. Ricci, A., Allende, A., Bolton, D., Chemaly, M., Davies, R., Fernández Escámez, P.S., Girones, R., Herman, L., Koutsoumanis, K., Nørrung, B., Robertson, L., Ru, G., Sanaa, M., Simmons, M., Skandamis, P., Snary, E., Speybroeck, N., Ter Kuile, B., Threlfall, J.,… Lindqvist, R. (2018) Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA Panel on Biological Hazards (Biohaz). EFSA Journal, 16:1–173. https://doi.org/10.2903/j.efsa.2018.5134
40. Sagun, E., Sancak, Y. C., İsleyici, Ö., & Ekici, K. (2001). The presence and prevalence of Listeria species in milk and herby cheese in and around Van. Turkish Journal of Veterinary & Animal Sciences, 25(1), 15-19.
41. Sanlıbaba, P., Tezel, B. U., & Cakmak, G. A. (2018). Detection of Listeria spp. in raw milk and dairy products retailed in Ankara. Gıda, 43(2), 273-282. https://doi.org/10.15237/gida.GD17107
42. Tasci, F., Turutoglu, H., & Ogutcu, H. (2010). Investigations of Listeria species in milk and silage produced in Burdur province. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16: 93-97.
43. Turhan, U. E. (2019). The presence of pathogenic bacteria in traditional cheese sold in local market in Hatay province, Turkey. Applied Ecology and Environmental Research, 17(3), 7135-45. http://dx.doi.org/10.15666/aeer/1703_71357145
44. Türkiye İstatistik Kurumu. Hayvancılık İstatistikleri Veri Tabanı (2022). Çiğ süt üretim istatistikleri. https://data.tuik.gov.tr/Bulten/Index?p=Cig-Sut-Uretim-Istatistikleri-2020-2021-45861.
45. Ulusoy, B. H., & Chirkena, K. (2019). Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the antibiotic resistance, Food Quality and Safety, 3(4), 233–241. https://doi.org/10.1093/fqsafe/fyz035
46. Wang, N. (2018). Conducting meta-analyses of proportions in R. Research Gate: College Station, TX, USA. World health Organization, WHO. (2018). Listeriosis, 20 February, 2018. https://www.who.int/news-room/fact-sheets/detail/listeriosis (Accessed 26 June 2023).
47. Yonar, H., Yonar, A., Mishra, P., Abotaleb, M., Al Khatib, A. M. G., Makarovskikh, T., & Cam, M. (2022). Modeling and forecasting of milk production in different breeds in Turkey. Indian Journal of Animal Sciences, 92(1), 105-111.
48. Yigin, A., Kılıc Altun, S., Demirci, M., Eser, N., & Yoldas, A. (2020). Utilization of real-time PCR method for identification of Listeria spp. from homemade white cheese originating from Southeast of Turkey. Applied Ecology and Environmental Research, 18(4), 5673-5682. http://dx.doi.org/10.15666/aeer/1804_56735682